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Microbial Biodiversity in Tasmanian Caves

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Microbial Biodiversity in Tasmanian Caves MICROBIAL BIODIVERSITY IN TASMANIAN CAVES Big Stalagmite, En trance Cave, Tasmania. Photograph taken by Jodie van de Kamp. Jodie Lee van de Kamp, B.Sc. (Hons) Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy The University of Tasmania Hobart, August, 2004 Declaration I declare that this thesis contains no material which has been accepted for the award of any other degree or diploma in any tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference is made in the text of this thesis. Jodie Lee van de Kamp 25th August 2004 2 Authority of Access This thesis may be made available for loan and limited copying in accordance with the Copyright Act, 1968. Jodie Lee van de Kamp 25th August 2004 3 ABSTRACT Caves represent one of few remaining isolated planetary habitats, in terms of human impact and characterisation of microbial biodiversity. Caves are unique environments characterised by little or no light, low levels of organic nutrients, high mineral concentrations and a stable microclimate providing ecological niches for highly specialised organisms. Caves are not uniform environments in terms of geological and geochemical characteristics, as they can vary from one to the other, eg. rock type, method of formation, length, depth, number of openings to the surface, presence or absence of active streamways, degree of impact by human visitation etc. Furthermore, on a smaller scale, various microhabitats, with vast differences in community structure can exist within caves. Culture studies point to the dominance of actinomycetes in caves and reveals great taxonomic diversity within actinomycetes isolated. However it is widely accepted that only - 1 % of microbes are cultured in the laboratory. Culture-independent methods are being increasingly used to describe the composition of microbial communities and reveal significantly broader diversity than culture-based studies. Nevertheless, to date our knowledge of bacterial communities in caves is largely due to culture studies. Based on the literature available, this study was initially aimed at examining culturable vs. non-culturable diversity of actinomycetes in Entrance and Loons Caves and to gain an increased understanding of the composition of cave microbial communities employing classical isolation and advanced molecular detection methods. As the study progressed the focus evolved as it became apparent that actinomycetes dominated only very specific habitats, the dry sediment in Entrance Cave, and represented only a minor fraction of the microbial biodiversity of most other microhabitats studied. Entrance Cave dry sediments and inactive (dry) speleothems produced a higher number of actinomycete isolates compared to saturated sediments and wet formations from Entrance and Loons Caves. This was reinforced by the actinomycetes being the second most abundant group (26.8%) detected in clone analysis of the dry Entrance sediment and low abundances (4-16%) detected in saturated sediments from both Entrance and Loons Caves. Sediment phylotypes and isolates identified in this study closely resemble species associated with oligotrophic, chemolithotrophic and heterotrophic lifestyles indicating that these communities survive by utilising a combination of metabolic pathways. Bacteria involved in the nitrogen and sulfur cycles were important members of all sediment communities along with hydrogen-oxidising bacteria. Pair-wise comparisons of sediment communities demonstrated that they were more similar to each other within individual cave systems, Entrance and Loons, rather than between microhabitat types (dry vs. wet sediment) though saturated sediment from Entrance Cave did show a higher degree of similarity in community composition to Loons Cave samples than the dry sediment from Entrance Cave. Saturated sediments were dominated by oligotrophs able to fix atmospheric gases, methanotrophs and had a high proportion of rare phylotypes most likely representing new 4 lineages related to microbes detected in anaerobic, anoxic environments, but low abundances of heterotrophic microbes. Geornicrobiological activities are no longer underestimated since studies have shown that bacterial metabolism may lead to mineral precipitation or dissolution. Questions remain as to the identity of these microbes and whether they are actively involved in speleothem formation, or simply buried during mineral precipitation. Results demonstrated a marked difference between sediment communities and those associated with calcite speleothem and calcite mat samples. Results of ESEM and XRD analysis demonstrated that calcite speleothem samples ME3 and MXl are true calcite moonrnilk (mondmilch). Phylogenetic analyses and isolation results demonstrated the unique composition of the microbial communities associated with moonrnilk deposits, predominantly composed of nitrogen-fixing ~-Proteobacteria and psychrotrophic heterotrophic CFBs and to a lesser extent, heterotrophic actinomycetes. Despite XRD and ESEM analysis showing similar calcite composition and crystal morphology, phylogenetic results indicated that sample ME2 represented a very different rnicrohabitat to moonmilk samples, dominated by oligotrophic a.-Proteobacteria and heterotrophic actinomycetes composing 84.2% of the total diversity. Phylogenetic analyses and biodiversity indices reveal the striking similarities between moonmilk samples from both Entrance and Exit Caves and the uniqueness of the calcite mat in Entrance Cave. The one similarity in composition between all three calcite communities was the presence of members of the Pseudonocardineae in particular of the genus Saccharothrix, in all calcite samples. 165 rRNA gene sequencing of cave isolates detected high levels of diversity and novelty, particularly of moonrnilk isolates. A total of two putatively novel genera (within the CFBs and Actinobacteria) and 18 putatively novel species (of genera: Paracoccus, Actinoplanes I Couchioplanes, Micromonospora, Amycolatopsis, Saccharothrix, Bacillus, Paenibacillus, Methylobacterium, Porphyrobacter, Sphingomonas, Alcaligenes, Stenotrophomonas, Xanthomonas) were identified. This study represents the first reported culture-independent analysis of moonrnilk microbial communities globally and of cave sediment communities in the Southern Hemisphere. Information gained from this study and the discovery of actively growing microbial communities appearing to precipitate CaC03 provides focus for important future studies and represents a unique opportunity to examine the nature and extent of complex microbe-mineral interactions in the formation of speleothems and implications for cave management. The biodiversity described acts as a baseline for assessing environmental impacts and to identify factors influencing microbial biodiversity. 5 ACKNOWLEDGEMENTS I would like to sincerely thank the following people: The University of Tasmania, Australian Biological Resources Study and Tasmanian Institute of Agricultural Research for funding that not only made this project possible but also allowed the work to be presented at several conferences, both nationally and internationally. National Parks and Wildlife Service, Tasmania, for in-kind support of the project including permits, data and advice. Supervisors, Dr. David Nichols and Dr. Kevin Sanderson, for managing to capture my interest in the project, open doors for me and remain focused to the end. Tom McMeekin, Tom Ross, Mark Brown, Adam Smolenski, Sharee McCammon, David Steele, Ralph Bottril, Susan Turner, Olivier Brassiant, Jill Rowling, Bill Cohen, Brendon Bateman and particularly John Bowman and Diana Northup, for technical expertise, excellent advice and helping me find direction when needed. The School of Agricultural Science, particularly the fantastic Microbiology Group, for providing endless opportunities, support and so many fond and entertaining memories. Including, but not solely, Kathleen Shaw, Guy Abel, Andrew Bisset, Matthew Smith, Shane Powell, Liv McQuestin, Laurie Parkinson, Andy Measham, Jane Weatherly, Heather Haines and Jimmy Twin. Special thanks to Lyndal Mellefont, Kristen Stirling and Craig Shadbolt. On a personal note, I am truly amazed at the overwhelming support from everyone in my life, I value that friendship more than you'll ever realise. There are so many people to thank, but special notes to, Kriss and Sarah Lawler, Mark van den Berg, Mark Jones, Nat Doran, Hill-Streeters Andy Wilson, Lee-Roy Evans and Kath Fearnley-Sander, Bee Hart, the Marauders, especially my girls and Sonya Enkleman, and for keeping me sane all these years, Tracey Brewer and Miss Holly Taylor. My wonderful extended family for so much love, support and unquestioning faith that I will succeed. My parents, Lorraine and Peter van de Kamp, my siblings, Jas, Brad, Laura and Steven, and their partners, Megs, Bridg and Justie, who never quite understood why I stayed at 'school' for so long, but have always been there for me. Finally, and certainly not least of all, Brendon, who always does what he can to help, has put up with me over these last few months without complaining (much©) and most of all is so full of support for the next stage of the journey. Thank you. 6 TABLE OF CONTENTS MICROBIAL BIODIVERSITY IN TASMANIAN CAVES ................................... 1 SECTION 1: ..................................................................................................................... 9 LITERATURE
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